Greven J.mann Cleven.p65

Transcription

Dentition in Ranodon sibiricus Kessler
195
Acta Biologica Benrodis 13 (2006): 195-217
Dentigerous bones, dentition and dental laminae in
the hynobiid salamander Ranodon sibiricus Kessler,
1866 (Amphibia, Urodela)
Zahntragende Knochen, Bezahnung und Zahnleisten bei dem
Hynobiiden Ranodon sibiricus Kessler, 1866 (Amphibia, Urodela)
HARTMUT GREVEN1, NORBERT JÖMANN2, GÜNTER CLEMEN2
1
Institut für Zoomorphologie und Zellbiologie der Universität Düsseldorf,
Universitätsstraße 1, D-40225 Düsseldorf, Germany; [email protected]
2
Institut für Evolution und Ökologie der Tiere der Universität Münster, Hüfferstraße 1,
D-48149 Münster, Germany
Summary: Among Urodela the hynobiids appear to be an ancient lineage, which seem to have
conserved several plesiomorphic characters. Such ancestral characters might also include dental
pattern and dentition. Using scanning electron microscopy and histological sections, the tooth
systems of larvae, juveniles and adults of the hynobiid salamander Ranodon sibiricus were documented and briefly compared with the tooth systems of other Urodela. Adults had three (upper
jaw arcade, lower jaw arcade, and the paired vomers), larvae had five tooth systems, those retained
in the adults and the paired palatines and coronoids (splenials of some authors) including their
dental laminae. The palatine of our youngest larva bore two rows of teeth, all other dentigerous
bones bore a single row of teeth. Post-metamorphosed specimens largely retained the larval pattern, i.e. single rows of teeth and replacements posterior to the tooth rows in labial direction.
Attachment of teeth was horizontal and more or less pleurodont depending on the particular bone
and numbers of previous dentitions. Succession of differently shaped tooth generations followed
the typical urodele pattern from larval “non-pedicellate” monocuspids via several, larval “subpedicellate” monocuspids to metamorphosed pedicellate bicuspids in a particular order. Even in the
adult, bicuspidity of teeth and shaping of the zone of division separating the crown from the
pedicle varied considerably. In larvae with a delayed metamorphosis the palatines were edentulous.
In the upper jaw arcade no gap was seen in the tooth row between the two premaxillae and the
premaxillae and maxillae indicating a single continuous dental lamina; in the lower jaw the edentulous gap between the dentaries argues for two dental laminae. Histological sections reveal clearly
separated vomerine and palatinal dental laminae in larvae. Already before regression of the palatine
and the coronoid, dental laminae of the two bones became regressive, the coronoid lamina later
than the palatinal one. Dental systems as realized in larval and metamorphosed R. sibiricus are
widespread among Urodela and appear to represent a highly conserved character.
Urodela, dentition, tooth systems, larval and transformed teeth, delayed metamorphosis, dental laminae, conserved character
Zusammenfassung: Innerhalb der Urodelen gelten Hynobiiden als altertümliche Gruppe, die
eine Reihe plesiomorpher Merkmale konserviert zu haben scheinen; dazu gehören wahrscheinlich
auch das Bezahnungsmuster und die Bezahnung selbst. Anhand von rasterelektronenmikroskopischen Aufnahmen und histologischen Schnitten beschreiben wir noch einmal die Zahnsysteme von
einige Larven, Juvenilen und Adulti des Hynobiiden Ranodon sibiricus und vergleichen diese kurz mit
den Zahnsystemen anderer Urodelen. Die Erwachsenen haben drei (Oberkieferbogen, Unterkie-
Acta Biologica Benrodis 13 (2006)
196
HARTMUT GREVEN, NORBERT JÖMANN & GÜNTER CLEMEN
ferbogen, paarige Vomeres), Larven jedoch fünf Zahnsysteme, und zwar die, welche vom Adulten
nach der Metamorphose zurückbehalten werden sowie die paarigen Palatina und Coronoide (die
Splenialia mancher Autoren) jeweils mit ihren Zahnleisten. Die Palatina der jüngsten uns zur
Verfügung stehenden Larven trugen zwei Zahnzeilen, alle übrigen zahntragenden Knochen jedoch
nur eine Zahnzeile. Metamorphosierte Exemplare behalten weitgehend das larvale Muster bei, d.h.
eine Zahnzeile sowie Zahnersatz in labialer Richtung hinter der Zahnzeile Die Verankerung der
Zähne ist in Abhängigkeit von Knochen und der Anzahl vorangegangener Dentitionen horizontal
sowie mehr oder weniger pleurodont. Die Abfolge unterschiedlich gestalteter Zahngenerationen
folgt dem typischen bei Urodelen verwirklichtem Muster von larvalen einspitzigen Zähnen ohne
abgesetzten Sockel über larvale einspitzige Zähne, bei denen die Grenze zwischen Sockel und
Krone nur angedeutet ist, bis zu metamorphosierten zweispitzigen Zähnen mit einem durch eine
Ringnaht deutlich abgesetzten Sockel. Bei den Adulti sind Ausprägung der Zweispitzigkeit und
Erscheinungsbild der Ringnaht sehr variabel. Bei zwei Larven, deren Metamorphose offenbar
verzögert war, waren die Palatina bereits zahnlos. Der Oberkieferbogen hat eine durchgehende
Zahnzeile und daher wahrscheinlich auch eine Zahnleiste, welche die beiden Prämaxillaria sowie
die Grenze zwischen Prämaxillare und Maxillare lückenlos begleitet, während zwischen den beiden
Dentalia im Unterkiefer eine solche Lücke in der Zahnzeile vorhanden ist. Die Zahnleiste entlang
des larvalen Vomer und Palatinum ist deutlich getrennt. Bereits vor dem metamorphosebedingten
Abbau des Palatinum und des Coronoid werden deren Zahnleisten regressiv, und zwar die des
Coronoids später als die des Palatinum. Die für larvale und metamorphosierte R. sibiricus hier
beschriebenen Zahnsysteme sind weitgehend identisch bei einer großen Zahl von Urodelen verwirklicht. Es scheint sich um hoch konservierte Merkmale zu handeln.
Urodela, Bezahnung, Zahnsysteme, larvale und metamorphosierte Zähne, verzögerte Metamorphose, Zahnleisten, konservierte Merkmale
1. Introduction
Previous studies have examined the pattern
of dentition of representative members of
extant paedomorphic and post-metamorphosed Urodela to show the variation of this
pattern, the diversity of tooth shapes during
ontogeny (summarized in CLEMEN & GREVEN 1994) and most thoroughly studied by
DAVIT-BEAL et al. (2006) focusing on ontogenetical changes of a single tooth family (for
review see also DAVIT-BEAL et al. 2007), the
course of dental laminae (not considered systematically as yet; see also DAVIT-BEAL et al.
2007) and the site of tooth replacement. Some
of these features are considered to be valuable tools for phylogenetical considerations for
a long time (for review see CLEMEN & GREVEN 1994). According to these studies three
“tooth systems” can be distinguished in postmetamorphosed salamanders: (1) the upper
jaw arcade consisting of the paired premaxilla
and maxillae and the accompanying conti-
nuous dental lamina; (2) the lower jaw arcade
formed by the paired dentaries accompanied
by a dental lamina that is interrupted in the
symphyseal zone; and (3) the vomerine system consisting of the two vomers, each accompanied by a dental lamina. In larvae and
some paedomorphic forms, two further systems are present: the palatinal portions of the
paired palatopterygoids and the paired coronoids each with their dental laminae. Teeth
were typically monocuspid and “non pedicellate” in early larvae and bicuspid and pedicellate in transformed specimens. In this case the
tooth consists of a crown that articulates with
a basal pedicle; crown and pedicle develop in
the enamel organ. These patterns appear rather
constant among Urodela; deviations primarily
concern the vomerine system and the number
of tooth rows established on the bones.
Among Urodela, the Hynobiidae are characterized by several plesiomorphic traits, e.g.,
external fertilization and a separate angular
bone in the lower jaw (e.g. SCHMALHAUSEN
1968; HECHT & EDWARDS 1977; LARSON &
DIMMICK 1993; GAO & SHUBIN 2001; LARSON
et al. 2003) and are considered as an ancient
lineage of extant urodeles. Within Hynobiidae
morphological analyses (ZHAO et al. 1988) and
molecular data (LARSON et al. 2003) are inconsistent, but more recently complete sequences
of mitochondrial genomes indicate convergent development of several morphological
characters in different hynobiid lineage. Further, Onychodactylus appears to be the sistergroup of all other living hynobiids (ZHANG
et al. 2006).
Skull ontogeny including the dentigerous
bones and dentitional pattern of the endangered (see IUCN 2006) hynobiid species, Ranodon sibiricus, is amazingly well studied (see particularly the summarizing work by LEBEDKINA
1979, now available in an English translation,
LEBEDKINA 2005). VASSILIEVA & SMIRNOV (2001)
re-examined LEBEDKINA's (l.c.) stained and
cleared specimens that cover a nearly complete ontogenetic series with regard to the succession of teeth from hatchlings to adults.
Authors revealed the sequence of structurally
different tooth generations, i.e. “non-pedicellate”, monocuspid teeth precede “subpedicellate” monocuspids in larvae that start
active feeding, pedicellate teeth in and after
metamorphosis, and pedicellate bicuspid
teeth after metamorphosis, a pattern known
from a variety of transforming Urodela (see
also GREVEN 1989; CLEMEN & GREVEN 1994;
DAVIT-BEAL et al. 2007). More recently JÖMANN
et al. (2005) published some supplementing
data on the skull, in particular of larvae with
a delayed metamorphosis, and included a few
notes on dentition.
In the present study a survey is given on
some aspects of dentitional ontogeny in R.
sibiricus, which is based on the literature and
examination of the material used in our previous study on cranial ontogeny (JÖMANN et
al. 2005). We show dentition of all developmental stages available to us by means of
scanning electron micrographs despite the risk
of reiteration. Unlike VASSILIEVA & SMIRNOV
197
(2001), we focus on the apex and the zone of
division that separates the crown from the
pedicle and on the attachment of teeth to the
dentigerous bones. In addition, we include
some histological sections to follow the course of dental laminae in the mouth roof and
briefly touch on possible plesiomorphic traits
in the tooth systems.
2. Material and methods
The material examined corresponds largely
to that used in a previous article (JÖMANN et
al. 2005, herein also a more detailed characterisation and staging of the specimens according to the tables of LEBEDKINA 1979, 2005;
KUZMIN & THIESMEIER 2001). We studied (nr.
1) larva (38 mm TL, stage 16); (nr. 2) larva at
the beginning of metamorphosis (41 mm
TL, stage 16-17); (nr. 3) larva in metamorphosis (60 mm TL, stage 19); (nr. 4) larva in
advanced metamorphosis (only the head was
available); (nr. 5, 6) larvae with delayed metamorphosis (67 and 73 mm TL, stage 19); (nr.
7) juvenile (75 mm, stage 20); (nr. 8) subadult (95 mm TL, stage 22); and (nr. 9) adult
(approx. 112 mm TL).
Scanning electron microscopy (SEM): Dentigerous bones were excised from the stained
and cleared specimens used in the previous
article (JÖMANN et al. 2005) and the tissue was
removed by 1% pancreatin in tetraborate buffer. The cleaning process was regularly controlled and the time needed for cleaning varied
considerably. We did not use any other macerating agent to save the delicate bones and
teeth especially in the younger stages. Nevertheless, cleaning did not satisfyingly succeed
in all preparations. During this procedure replacement teeth and largely resorbed teeth
were lost. Further, specimens may have suffered of some demineralisation.
A single head of a larva in an advanced
stage of development (palatine teeth were
already missing) (larva nr. 4 a; nearly stage 18;
no further data available and not listed above),
fixed in 2.5% glutaraldehyde in 0.1 M cacody-
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late buffer and embedded in paraplast was
freed from paraplast. All preparations were
dehydrated in an ascending ethanol series, critical-point dried, sputtered with gold and
examined in a Hitachi-Scanning Electron
Microscope.
Heads of a larva in metamorphosis (larva
3 a; nearly stage 19; no further data available
and not listed above) and a larva with delayed (90 mm TL; larva 6 a; nearly stage 19)
fixed in glutaraldehyde or neutral formaldehyde, respectively, were embedded in paraplast, sectioned transversally at 7 µm and
stained with Azan or Trichrom-Goldner
(ROMEIS 1989).
3. Results
3.1. Larva (nr. 1) (Figs 1a-f)
Toothed bones were premaxillae, vomers,
palatines (=anterior palatinal portion of the
palatopterygoid; homology with the palatine
of other vertebrates is doubtful, e.g. SCHOCH,
1998), dentals and coronoids.
Premaxillae (Fig. 1 a), vomers (Fig. 1 b),
dentaries (Fig. 1 d), and coronoids (Fig. 1f)
bore a single row of teeth (monostichous
dentition), whereas the palatine has two rows
(bistichous dentition) (Fig. 1 c).
Teeth of all bones were ankylosed with a
broad base. The basis of dentary teeth was
thickened lingually (Fig. 1 d). Attachment varied from nearly acrodont, i.e teeth are attached
more or less horizontal on the surface of the
bone (vomer, coronoid, palatine) to slightly
pleurodont, i.e. teeth are attached by one side
to the inner surface of the bone (dentary, premaxilla). Openings to the pulp varied in size
and shape ranging from a large opening (premaxilla: Fig. 1a), and several small accesses
(vomer: Fig. 1 b, palatine: Fig. 1 c; dentary:
Fig. 1 d; coronoid: Fig. 1 f).
Teeth were monocuspid, undivided and
were curved more or less lingually with the
exception of coronoid teeth, which were
straight (Fig. 1 f).
3.2. Larva at the beginning of metamorphosis (nr. 2) (Figs 2a-i)
Dentigerous bones as in the previous stage.
The disintegrating anterior and median portion of the palatine was toothless (Fig. 2 f).
All bones including the palatine bore a
single row of teeth. Size and shape of teeth
vary considerably even on the same bone (Fig.
2). On the premaxilla and dentary the most
posterior teeth were smaller and sturdy, more
anteriorly, teeth were slender and curved more
or less inwards (Figs 2 a, c, g).
Ankylosis has changed to a pleurodont condition (premaxilla: Fig. 2 a; dentary: Fig. 1 g).
In the latter the bases of teeth was wider than
the shaft (Fig. 2 c). On the other bones ankylosis was horizontal and teeth were broadbased. Premaxillary teeth had a larger pulpal
access (Fig. 2 b) than vomerine, dentary and
coronoid teeth, which showed several
smaller openings.
Teeth were monocuspid and undivided.
Teeth showed at best a globular ring between the basis and the crown (e.g. dentary:
Fig. 2 g).
3.3. Larvae in metamorphosis (nr. 3)
(Figs 3a-h)
Premaxillae, maxillae, vomers, and dentaries
bore a single row of teeth. Palatines and coronoids were largely disintegrated. The palatines
were entirely toothless. The coronoid showed
resorption pits (Fig. 3 g). Ankylosis of teeth
largely as in the previous stage. Dentition of
maxillaries was pleurodont (Fig. 3 a), that of
the vomers slightly pleurodont due to remnants of previous dentitions (Fig. 3 e).
Pulpal accesses were large and few (premaxilla,
maxilla, dentary: Figs 3 a, d, f) or smaller and
more numerous (vomer: Fig. 3 e).
Teeth of the premaxilla, maxilla and dentary were monocuspid and incipiently divided
(Fig. 3 a, f), teeth of the vomer, however,
monocuspid and undivided (Fig. 3 e). The
zone of division was more distinct lingually
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Figs 1 a-f: Larva nr. 1. a Premaxillary teeth, lingual view, with broad basis and slight pleurodont
attachment. b Vomerine tooth, lingual view. c Palatine with two rows of teeth, bases touch one
another, caudal view. d Dentary, lingual view; attachment of teeth is more or less pleurodont and
teeth are widely separated. e Dentary, medio-lingual view; broad-based tooth. f Straight coronoid
tooth with signs of basal resorption.
Abb. 1 a-f: Larve nr. 1. a Prämaxillarzähne, lingual, mit breiter Basis und leicht pleurodonter
Verankerung. b Vomerzahn, lingual. c Palatinum mit zwei Zahnzeilen. Die basalen Abschnitte der
Zähne berühren sich fast, caudal. d Dentale, lingual; mehr oder weniger pleurodonte Verankerung
der weit voneinander getrennen Zähne. e Dentale, medio-lingual, mit breitbasigen Zähnen.
f Gerader Zahn auf dem Coronoid mit Resorptionsnarben an der Basis.
200
Figs 2 a-i: Larva at the onset of metamorphosis (nr. 2). a Premaxillary, lingual view; with
pleurodont dentition. The more posterior teeth (left side) differ in size and shape from the median
ones (right side). b Tooth of the median premaxilla, lingual view, with pulp opening (asterisk). c
Posterior sturdy premaxillary tooth; the basis is thickened (arrow). d Anterior outgrowth of the
vomerine plate (asterisk); the missing portion of the vomerine plate (arrowhead) is an artefact. e
Vomerine tooth, medio-lateral view, with enamel cap; prospective dividing zone (arrow). f Monostichous dentition of the palatine, top view, caudal; toothless anterior (arrowheads) and median
disintegrating portion (arrow); bony bridge between the palatine and the pterygoid (asterisk). g
Dentary, lingual view; posterior teeth (arrow) are smaller as the anterior and more curved. h
Coronoid, lingual view, with horizontally ankylosed teeth. i Coronoid tooth, lingual view, with
boundary between the basis and the bone (arrow).
Abb. 2 a-i: Larve am Beginn der Metamorphose (nr. 2). a Prämaxillare, lingual, mit pleurodont
verankerten Zähnen. Die hintersten Zähne (links) unterscheiden sich von den mittleren (rechts). b
Zahn aus der Mitte des Prämaxillare, lingual; Öffnung zur Pulpa (Stern). c Hinterer untersetzter
than labially (Figs 3 a, b). The surface of the
teeth became rougher in the direction of the
dividing zone (dentary, Fig. 3 f). The single
tooth established on the coronoid was monocuspid and undivided; the shaft above the
broad basis appeared waisted, perhaps a result
of a partial demineralisation (Figs 3 g, h).
Pedicles were bulged at the lingual side, but
were not broadened significantly (premaxilla,
maxilla, dentary). They were distinctly separated from the zone of ankylosis and did not
touch each other. Teeth were bent inwards,
i.e. lingually (Figs 3 c and d), or were nearly
straight (dentary: Fig. 3 f).
3.4. Larva in an advanced stage of metamorphosis (nr. 4 and 4 a) (Figs 4 a-i)
Number of rows, ankylosis of teeth and
pulpal accesses as in the previous stage; coronoids regressive and without teeth.
In the upper jaw dentition was continuous
without a gap in the symphyseal zones between the premaxillae and between premaxilla/maxilla; vomers did not have contact
each other; their partes dentales were situated
in the midst of the bone and their laterocaudal edges lied at the level of the choana (that
mark the lateral boundary of each vomer)
(Figs 4 a, e-g).
Teeth were either bicuspid and divided (premaxilla: Figs 4 b, c), monocuspid and divided
(maxilla: Fig. 4 d), monocuspid and incipiently divided posteriorly or bicuspid and
divided anteriorly (dentary: Figs 4 h, i) or
monocuspid and undivided (vomer: Figs 4 e
-g). On the dentary, the anterior teeth near
the symphysis were larger and bicuspid. Pos-
201
teriorly teeth became smaller and were monocuspid and broad-based (Fig. 4 h, right side).
Each tooth had a large dominant lingual
opening to the pulp (Fig. 4 d, h) or a larger
and several small (vomer, Figs 4 e-f). Teeth
were curved inwards; in the bicuspids, two
cusps were of nearly equal size (Figs 4 c, i).
3.5. Larva with delayed metamorphosis
(nr. 5 and 6) (Figs 5 a-l)
Premaxillae, maxillae, vomers, dentaries and
coronoids with a single row of teeth; palatine regressive without teeth. Dentition was
pleurodont (premaxillae, maxillae, dentaries),
slightly pleurodont (on the vomer; the pars
dentalis was now situated in the posterior third
of the vomer: Figs 5 e,d f) or broad-based
and nearly horizontal (coronoid: Fig. 5 k, l).
Large pulpal accesses were seen in the teeth
attached in a pleurodont condition and
smaller and more numerous accesses in teeth
attached horizontally (Fig. 5 g). Teeth were all
monocuspid with an dividing zone indicated
by a globular surface (maxilla: figs 5 d). Transversal ridges (premaxilla: Fig. 5 a), incisions
(dentary: Fig. 5 j) or a waist (Fig. 5 k, l) might
be a result of partial demineralisation..
3.6. Juvenile specimen (nr. 7) (Figs 6 a-i)
Number of tooth rows, ankylosis of teeth
and pulpal accesses as in larva nr. 4 (see
above); coronoids no longer present. Vomerine teeth shifted near the posterior edge of
the bone (Fig. 6 f).
Teeth of all dentigerous bones were bicuspid and divided (premaxilla, maxilla: Figs
Prämaxillarzahn mit verdickter Basis (Pfeil). d Vorderer Bereich der Vomerplatte (Stern); ein Teil
der Vomerplatte (Pfeilkopf) ist präparationsbedingt nicht mehr vorhanden. e Vomerzahn, mediolateral, mit Schmelzkappe und prospektiver Ringnaht (Pfeil). f Einzeilige Bezahnung des Palatinum, Aufsicht; zahnloser vorderer (Pfeilköpfe) und mittlerer im Abbau begriffener Teil (Pfeil);
Knochenbrücke zwischen Palatinum und Pterygoid (Stern). g Dentale, lingual; die hinteren Zähne
(Pfeil) werden kleiner und sind gekrümmter. h Coronoid, lingual, mit horizontal verankerten
Zähnen. i Zahn auf dem Coronoid, lingual, mit deutlicher Grenze zwischen Basis und Knochen
(Pfeil).
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Figs 3 a- h: Larva in metamorphosis (nr. 3). a Premaxillary, lingual view; attachment of the lingually
curved teeth is slightly pleurodont; teeth have a large pulpal access each (arrow). b Incipient dividing
zone (arrowhead) of a premaxillary tooth, lingual view. c Apex of a maxillary tooth. d Maxillary teeth
with large pulpal accesses (arrows); processus facialis maxillaris (asterisk). e Vomer, lingual view; labial
remnants of previous dentitions (arrows); pars palatina (asterisk). f Dentary, lingual view; putative
divided (arrows) teeth are attached in a pleurodont condition; large pulpal openings (asterisks). g Single
coronoid tooth, lingual view; resorption of the coronoid (sp) from posterior (below) to anterior (on the
top); prearticular (pa). h Detail of figure g. Straight “non-pedicellate” coronoid tooth.
Abb. 3 a-h: Larve in der Metamorphose (nr. 3). a Prämaxillare, lingual; die Zähne sind lingual
gekrümmt, pleurodont verankert und haben einen großen Zugang zur Pulpa (Pfeil). b Sich bildende
Ringnaht (Pfeilkopf) eines Prämaxillarzahnes, lingual. c Spitze eines Maxillarzahns. d Maxillarzahn
mit großen Pulpazugängen (Pfeile); processus facialis maxillaris (Stern). e Vomer, lingual: labiale Reste
früherer Dentitionen (Pfeile); pars palatina (Stern). f Dentale, lingual; die geteilten Zähne sind pleurodont verankert und haben große Pulpaöffnungen (Sterne). g Einzelner Zahn auf dem Coronoid,
lingual; Resorption des Coronoids (co) von hinten (unten) nach vorn (oben); Präarticulare (pa). h
Ausschnitt aus Abbildung g. Gerader nicht zweigeteilter Zahn auf dem Coronoid.
Figs 4 a-i: Larvae in an advanced stage of metamorphosis (nr. 4, 4a); preparations with (a, c, g) and
without (b, d-f, h, i) soft tissue. a Premaxillae and vomers, symphyseal region (arrow on the top) with
continuous dentition, lingual view; vomers (arrowhead); gap between vomers (arrow); choana (aste-
203
risk). b Premaxillary teeth with incipient bicuspidity (arrowheads) and zone of division (arrow). c A
bicuspid (arrow) and monocuspid tooth side by side in the upper jaw, frontal view. d Maxilla with
lingually curved teeth attached in pleurodontous condition; processus facialis maxillaris (asterisk). e
Vomer; pars dentalis with remnants of previous dentitions (arrow) in the middle; vomerine plate (arrowhead) and pars palatina (asterisk). f Monocuspid vomerine teeth; pulpal access (asterisk); Howship
lacunae in the pedicle (arrow). g Monocuspid vomerine teeth penetrating the oral epithelium; taste buds
(arrowheads), lingual. h Dentary, lingual view; the posterior teeth (arrows) are monocuspid, the anterior
tooth (arrowhead) is bicuspid. i Apex of an anterior bicuspid dentary tooth with distinct enamel cap.
Abb. 4 a-i: Larve in fortgeschrittenem Stadium der Metamorphose (nr. 4, 4a). Präparate mit (a, c, g) und
ohne (b, d-f, h, i) Weichgewebe. a Prämaxillaria und Vomeres; Symphysenregion (Pfeil oben) mit einer
lückenlosen Bezahnung, lingual; Vomeres (Pfeilkopf); Lücke zwischen den Vomeres (Pfeil); Choane
(Stern). b Prämaxillarzaähne mit Anzeichen von Zweispitzigkeit (Pfeilköpfe) und Ringnaht (Pfeil). c
Benachbarter bicuspider (Pfeil) und monocuspider Zahn im Oberkiefer, von vorn. d Maxillare mit
lingual gekrümmten, pleurodont verankerten Zähnen; processus facialis maxillaris (Stern). e Vomer; pars
dentalis mit Resten früherer Dentitionen (Pfeil) inmitten der Vomerplatte (Pfeilkopf); pars palatina
(Stern). f Monocuspide Vomerzähne; Pulpazugang (Stern); Howshipsche Lakunen im Sockel (Pfeil). g
Monocuspider Vomerzahn durchdringt das Mundepithel; Geschmacksknospen (Pfeilköpfe). h Dentale,
lingual; monocuspide, hintere Zähne (Pfeile), bicuspider vorderer Zahn (Pfeilkopf). i Dentale; Apex
eines vorderen bicuspiden Zahnes mit deutlicher Schmelzkappe.
204
Figs 5 a-l: Larvae with delayed metamorphosis (nr. 5 and 6). a Premaxillary teeth, lingual view. b
Maxillary teeth, lingual view; a dividing zone can hardly be recognized; processus facialis maxillaris
(asterisk). c Apex of a maxillary tooth. d Maxillary tooth with a lingual bulge (left side) and
globular surface (asterisk). e Vomer with pars dentalis (arrows) shifted more caudally; vomerine
plate (arrowhead); pars palatina (asterisk) broken off (right side). f The anterior edge of the
vomerine pars dentalis with remnants of previous dentitions, labial view. g Vomerine tooth with a
broad basis and numerous small pulpal accesses. h Vomerine tooth with a worn-out apex. i Dentary
with pars dentalis; teeth attached in a pleurodont condition increase in height posteriorly. j Attachment of dentary teeth is pleurodontous, lingual view; zone of division (arrow). k Coronoid teeth,
lingual view, are horizontally attached. l Waisted coronoid tooth, lingual view.
Abb. 5 a-l: Larven mit verzögerter Metamorphose (nr. 5 und 6). a Prämaxillarzähne, lingual. b
Maxilarzähne, lingual; eine Ringnaht ist kaum zu erkennen; processus facialis maxillaris (Stern). c
Apex eines Maxillarzahnes. d Maxillarzahn mit lingualer Ausbuchtung (links) und globulärer Oberfläche (Stern). e Vomer mit pars dentalis (Pfeile) nach caudal versetzt; Vomerplatte (Pfeilkopf); pars
palatina (Stern) gebrochen (rechts). f Vordere Kante der pars dentalis des Vomer mit Resten früherer
Dentitionen, labial. g Vomerzahn mit breiter Basis und zahlreichen Pulpazugängen. h Vomerzahn
mit abgenutztem Apex. i Dentale mit pars dentalis; die pleurodont verankerten Zähne werden nach
hinten hin größer. j Pleurodont verankerte Zähne, lingual. Ringnaht (Pfeil). k Die Zähne auf dem
Coronoid sind horizontal veankert. l Zahn auf dem Coronoid mit Taille, lingual.
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Figs 6 a-i: Juvenile (nr. 7). a Premaxilla, lateral view; teeth have high, slender pedicles; dividing
zone (arrowheads). b Premaxillary tooth with a small, labial (arrowhead) and a slightly larger
lingual (arrow) sharp edged cusp. c Maxillary teeth with large pulpal accesses (arrowheads); processus facialis maxillaris (asterisk). d Pediclelate (arrow) maxillary teeth, lingual view. e Lingually
recurved maxillary teeth. f Vomer, lingual view; pars palatina (asterisk). g Slender vomerine teeth
with a globular dividing zone (arrow), lingual view. h Dentary, lingual view; teeth have slender and
long pedicles. i Dentary teeth, labial view; note the varying aspect of the dividing zone (arrows).
Abb. 6 a-i: Juvenis (nr. 7). a Prämaxillare, lateral; die Zähne besitzen hohe, schlanke Sockel;
Ringnaht (Pfeilkpfe). b Prämaxillarzahn with kleiner, labialer (Pfeilkopf) und geringfügig größerer
lingualer (Pfeil) scharfkantigen Spitze. c Maxillarzahn mit großen Pulpazugängen (Pfeilköpfe);
processus facialis maxillaris (Stern). d Maxillarzahn mit Sockel (Pfeil), lingual. e Lingual gekrümmter
Maxiallarzahn. f Vomer, lingual; pars palatina (Stern). g Schlanker Vomerzahn mit globulärer
Ringnaht (Pfeil), lingual. h Dentale, lingual; die Zähne sind schlank und haben lange Sockel. i
Zähne auf dem Dentale, labial, mit unterschiedlich ausgeprägter Ringnaht (Pfeile).
6 a, b, c; dentary: Figs 6 h, i; vomer: Figs 6 f, g).
The dividing zone in the upper jaw was lingually more distinct than labially (Figs 6 c-e).
In dentary teeth the dividing zone showed a
deep cleft at the labial side, whereas lingually
the cleft showed some material perhaps not
or weakly mineralized (Figs 6 h, i). The dividing zone of vomerine teeth was characterized
by a globular ring (Figs 6 f, g). Apices of teeth
were curved lingually and had two distinct
cusps, the labial one was smaller and sharper
than the lingual one (Figs 6 b, i). In a labial
view, slender pedicles towered above the anterior edge of the bone (Figs 6 i). Blades of
cusps in vomerine teeth were not clearly conspicuous (Fig. 6 g).
206
Figs 7 a-k: Subadult specimen (nr. 8). a Premaxilla, lingual view; processus dorsalis praemaxillaris
(asterisk). b Lingually curved premaxillary teeth with a small lingual dividing zone (arrowhead). c
Premaxillary tooth, lateral view, with differently shaped cusps; labial blade (arrowhead). d Maxilla.
e Maxillary teeth with a thin zone of division (arrowhead), lateral view. f Vomer; pars dentalis
(black arrow) between the pars palatina (asterisk) and vomerine plate (arrowhead); gap for the
choana (white arrow). g Anterior portion of the vomerine pars dentalis with remnants of previous
dentitions (asterisk), lateral view. h Vomerine tooth with a blunt lingual cusp (arrowhead). i
Dentary, lingual view, with ascending pars palatina (asterisk). j Dentary teeth are pleurodontously
attached. k Dentary tooth with greatly reduced labial blade (arrow).
Abb. 7 a-k: Subadultus (nr. 8). a Prämaxillare, lingual; processus dorsalis praemaxillaris (Stern). b
Lingual gekrümmte Prämaxillarzähne mit kleiner lingualen Ringnaht (Pfeilkopf). c Prämaxillarzahn,
207
3.7. Subadult (nr. 8) (Figs 7 a-k)
was covered with dense connective tissue that
amalgamated with the tunica propria.
In the larvae in metamorphosis and with
delayed metamorphosis (both approximately stage 19), the upper jaw arcade (premaxillae
and maxillae) had a single continuous dental
lamina at the lingual side. Due to the lack of
an adequate histological series, this is concluded by the fact that the symphyseal zones
between the two premaxillae and the premaxilla/maxilla were small and the tooth row
did not show any gap.
Vomers possessed their own dental lamina each. At the level of the choana (Fig. 9 a)
and posterior to the choana the dental lamina still produced tooth buds (Fig. 9b); before
disappearing it became one-layered and tooth
buds could not be seen (Fig. 9c). The posterior end of the vomerine dental lamina was
clearly separated from the palatinal dental lamina by connective tissue (Fig. 9 d). The palatinal dental lamina began with a process entirely surrounded by connective tissue (Fig. 9
e); more posteriorly its terminus fused with
the oral epithelium and was productive (Fig.
9 f). Beyond the last tooth bud, the unproductive dental lamina was shortened (Fig. 9
g). Posteriorly, the dental lamina disappeared,
although parts of the degenerating palatine
were still present (Fig. 9 h).
Number of tooth rows, ankylosis and curvature of teeth and pulpal accesses as in the
previous stage.
Teeth of all dentigerous bones were bicuspid and divided (Figs 7 a-k). The apex of
the teeth had two cusps, the labial one
smaller than the lingual. However, proportion between the two cusps varied considerably (see Figs 7 c, h, j, k).
3.8. Adult (nr. 9) (Figs 8 a-k)
Number of tooth rows, anchorage and curvature of teeth and pulpal accesses as in the
previous stage. In the upper jaw only maxillary teeth were available.
All teeth were bicuspid and divided (Figs 8
a-k). The dividing zone was deeper labially
than lingually (Figs 8 d, e, h) showing a small
ring like depression lingually (Fig. 8 k).
From the cusps, the labial one was significantly reduced (maxilla: Fig. 8 c; vomer: Fig. 8
f); both cusps may have blades (maxilla: Fig.
8 c). Teeth of the dentary showed a slight
reduction of the labial blade; the lingual cusp
was rounded off (Fig. 8 i). Here teeth were
strongly recurved, so that the larger blade was
nearly horizontal (Fig. 8 j); the most posterior tooth differed from the other teeth by its
broad pedicle, its sturdy shape and several 4. Discussion
pulpal accesses (Fig. 8 l).
4.1. Attachment and succession of
3.9. Dental laminae (Figs 9 a-h)
differently shaped tooth generations
Dental laminae are two layered derivates of
the stratum basale of the oropharyngeal epithelium. The face of the dental laminae
turned towards the oropharyngeal epithelium
Succession of differently shaped and divided
teeth described by VASSILIEVA & SMIRNOV
(2001) for Ranodon sibiricus and pictured herein for some stages more thoroughly closely
lateral, mit unterschiedlichen Spitzen; labiale Schneide (Pfeilkopf). d Maxillare. e Maxillarzähne mit
dünner Ringnahr (Pfeilkopf), lateral. f Vomer; pars dentalis (schwarzer Pfeil) zwischen pars palatina
(Stern) und Vomerplatte (Pfeilkopf); Lücke für die Choane (weißer Pfeil). g Vorderer Teil der pars
dentalis des Vomer mit Resten früherer Dentitionen (Stern), lateral. h Vomerzahn mit stumpfer
lingualer Spitze (Pfeilkopf). i Dentale, lingual mit aufsteigender pars palatina (Stern) .j Pleurodont
verankerte Zähne des Dentale. k Zahn des Dentale mit stark reduzierter labialer Schneide (Pfeil).
208
Figs 8 a-l: Adult specimen (nr. 9). a Maxillary, lingual view, and processus facialis maxillaris (asterisk). b Slender pedicles of maxillary teeth, lingual view. c Maxillary tooth, lingual view, with two
different cusps. d Zone of division of a maxillary tooth, lingual view. e Zone of division of a
maxillary tooth, labial view. f Apex of a vomerine tooth, lateral view. g Vomerine teeth with
distinct labial dividing zones (arrows); pars palatina (asterisk) and pars dentalis (arrowhead). h
Dividing zone of a vomerine tooth, lateral view. Note the incision labially (arrowhead). i Dentary
tooth with a blunt lingual cusp (arrowhead). j Lingually curved dentary teeth; note the varying
bicuspidity. k Zone of division in a dentary tooth, lateral view. l The most posterior tooth of the
dentary is sturdy, bicuspid and broad-based.
Abb. 8 a-l: Adultus (nr. 9). a Maxillare, lingual, und processus facilais maxillaris (Stern). b Schlanke
Sockel der Maxillarzähne, lingual. c Maxillarzahn, lingual, mit zwei unterschiedlichen Spitzen. d
Ringnaht eines Maxillarzahns, lingual. e Ringnaht eines Maxillarzahns, labial. f Apex eines Vomerzahns, lateral. g Vomerzähne mit deutlicher labialer Ringnaht (Pfeile); pars palatina (Stern) und pars
dentalis (Pfeilkopf). h Ringnaht eines Vomerzahns, lateral. Man beachte den labialen Einschnitt
(Pfeilkopf). i Zahn des Dentale mit stumpfer lingualer Spitze (Pfeilkopf). j Lingual gekrümmte
209
Figs 9 a-h: Dental laminae of the vomer (a-c), between vomer and palatine (d), and the palatine
(e-h); cross sections. a Dental lamina (arrow) with associated replacement tooth (arrowhead);
choana (asterisk). b Dental lamina at the level of the choana with tooth bud (arrow). c Before
disappearing posteriorly the dental lamina becomes one-layered (arrow). d Between vomer (asterisk) and palatine (arrow) a dental lamina is absent. e Free rostral end of the palatine dental lamina
in the subepithelial connective tissue (arrow). f Connection of the dental lamina with the oral
epithelium (arrow); most anterior tooth bud (arrowhead). g Short dental lamina (arrow) near the
palatine (p) approx. 7 µm behind the last tooth bud. h In the section following g the dental lamina
is absent; palatine (p).
Abb. 9 a-h: Zahnleisten des Vomer (a-c), zwischen Vomer und Palatinum (d) und Palatinim (e-h);
Querschnitte. a Zahnleiste (Pfeil) mit Ersatzzahn (Pfeilkopf); Choane (Stern). b Zahnleiste in
Höhe der Choane mit Zahnkeim (Pfeil). c Vor ihrem Verschwinden wird die Zahnleiste einschichtig (Pfeil). d Zwischen Vomer (Stern) und Palatinum (Pfeile) fehlt die Zahnleiste. e Freies rostrales
Ende der palatinalen Zahnleiste im subepithelialen Bindegewebe (Pfeil). f Verbindung der Zahnleite mit dem Mundepithel (Pfeil); hinterster Zahnkeim (Pfeilkopf). g Kurze Zahnleiste (Pfeil)
nahe des Palatinum (p) etwa 7 µm hinter dem letzten Zahnkeim. h Im Folgeschnitt ist die Zahnleiste nicht mehr vorhanden; Palatinum (p.).
Zähne des Dentale mit unterschiedlicher Zweispitzigkeit. k Ringnaht eines Zahns auf dem Dentale, lateral. l Der hinterste Zahn auf dem Dentale ist untersetzt, zweispitzig und breitbasig.
210
corresponds to that seen in the majority of
transforming Urodela (CLEMEN & GREVEN
1994; see DAVIT-BEAL et al. 2006, 2007): Tooth
germs appear at sites where the dentigerous
bones will develop in most cases already during the embryonic period. Anchorage of the
(functional) small, conical and undivided teeth
takes place during the mineralization process
of these bones (see also LEBEDKINA 2005)
and teeth are attached to the bones horizontally (palatine, vomer, coronoid) or slightly
pleurally (premaxilla, dentary). The mode of
ankylosis appears to be dictated by the shape
of the dentigerous bone and by the number
of previous dentitions. In our material a pleurodont ankylosis was seen on the premaxillae, maxillae and dentaries, obviously right
from the start but with increasing pleurodont
attachment in later stages. On the palatine
and coronoid teeth were always horizontally
attached, on the flattened vomer, however,
initially horizontally and later slightly pleurodont due to remnants of previous dentitions (see also CLEMEN & GREVEN 1979). Obviously, there is the tendency to reduce and
enlarge accesses to the pulp with an increasing pleurodont attachment. Broad-based
teeth seen on bones (e.g. dentaries, maxillae)
bearing anteriorly a pleurodont dentition, always were horizontally attached and showed
several pulpal accesses. Generally, the conical
teeth of very young urodele larvae have a small
non-vascularized pulp and a tubular dentine
(BOLTE et al. 1996). Such teeth were suggested to be conserved organs representing an
ancestral character for gnathostomes (SIRE et
al. 2002). In the majority of Urodela these
“early” larval teeth (undivided, conical, broadbased, monocuspid) are replaced by conical
monocuspids that may gradually change from
a “non-pedicellate” (a pedicle cannot be distinguished) to a pedicellate condition (the
pedicle is separated from the crown by a more
or less complete distinct zone of division) via
various intermediate stages named “subpedicellate” by some authors. Not until metamorphosis teeth become replaced by fully
divided (=pedicellate), bicuspid teeth, and
bicuspidity seems to develop also via intermediate stages. This was mentioned for instance in the articles of BENESKI & LARSEN
(1989 a, b) and (BOLTE & CLEMEN 1991) and
demonstrated unequivocally by DAVIT-BEAL
et al. (2006).
Terminology of these three major ontogenetic stages is inconsistent in literature. BENESKI & LARSEN (1989 b) distinguished in their
SEM-pictures “for clarity and consistency” (p.
166) 1) non-pedicellate teeth (stage I) with a
distal monocuspid apex (covered entirely by
enameloid) and a proximal shaft (not covered by enameloid), 2) subpedicellate teeth (stage II) with a distal monocuspid crown (only
its apex is covered by enameloid) and a proximal base separated from the crown by an abrupt increase in width and/or a lingual fibrous zone of division, and 3) pedicellate
teeth (stage III), with a distal crown consisting of the modified, i.e. bicuspid, apex, and
shaft (the apex is entirely covered by enamel,
the shaft only in its distal part), and a proximal pedicle separated completely by an annular zone of weakness (see Fig. 1 in BENESKI &
LARSEN 1989 b; see also VASSILIEVA & SMIRONOV 2001). Apart from the fact that the apex
of larval teeth probably possesses true enamel and enameloid instead of enameloid alone (see BOLTE & CLEMEN 1992; BOLTE et al.
1996; KOGAYA 1994, 1999; WISTUBA et al.
2002), this terminology, although adopted
by various researchers, does not meet the real
conditions and appears highly arbitrarily. By
definition non-pedicellate teeth do not show
a dividing zone between the distal and proximal part by LM and SEM. However, their
“proximal shaft” or base definitely lacks dentine tubules such as the pedicles of transformed teeth (BOLTE et al. 1996). That means
that early larval teeth possess a true pedicle.
Further, VASSILIEVA & SMIRNOV (2001) describe on the basis of their stained and cleared
specimens that mineralization of small nonpedicellate teeth begins from a single apical
mineralization centre and proceeds in apico-
basal direction, whereas mineralization of
“subpedicellate” and pedicellate teeth starts
from an apical and a basal centre moving in
apico-basal and basal apical direction, respectively. There is evidence by TEM-micrographs
that also in early larvae two mineralization
fronts exist (Ambystoma mexicanum: WISTUBA
et al. 2002).
Typically, in bicuspid teeth the lingual cusp
is elongated, but sharper than the labial one.
Compared to the relative time the dividing
zone develops, the change of the tooth crown
from monocuspids to bicuspids seems to
take place in a relatively shorter period around
metamorphosis.
Only in a few metamorphosed urodeles
teeth deviate from the bicuspid type; e.g., in
some Ambystoma species basic cusp shapes
of pedicellate premaxillary teeth are disc or
club (see BENESKI & LARSEN, 1989a), which,
however, all can be attributed to the bicuspid
type; male plethodontids have premaxillary
teeth that secondarily changed to cone-shaped
monocuspids under the influence of testosterone during the breeding season (e.g.,
NOBLE & POPE 1929; EHMCKE et al. 2003;
GREVEN et al. 2004).
In adult R. sibiricus the shape of the two
cusps of teeth is rather variable, mainly regarding the lingual cusp, which probably cannot
solely be attributed to the fact that bicuspidity develops gradually on the different dentigerous bones (see below). Also the zone of
division that creates the pedicellate condition
in metamorphosed urodele teeth and is considered an apomorphic character of extant
Amphibia (e.g., PARSONS & WILLIAMS 1962;
DUELLMAN & TRUEB 1986; GREVEN 1989; AX
2001; the latter author also gives reasons why
to cancel the term “Lissamphibia” used for
the extant Amphibia) shows a considerable
variation. A transverse annular zone of division was lacking in our youngest larva (and is
lacking also in earlier stages; see VASSILIEVA &
SMIRNOV 2001); in later stages this zone appears to be indicated only by a more or less
globular area around the tooth and curvature
211
of teeth might indicate the future region of
the dividing zone (e.g., DAVIT-BEAT et al. 2006).
Even in adults this zone was often remarkably less distinct when compared to other
metamorphosed urodeles. We don’t know,
whether this variability is a question of the
age of the animals, i.e. fully metamorphosed
and older adults may be expected to show a
more conspicuous zone division as seen in a
variety of Urodela, or caused by a heavier or
even secondary calcification of the collagenous
fibres bridging the gap between crown and
pedicle (MOURY et al. 1985; GREVEN et al. 1989;
WISTUBA et al. 2002). Regarding the ontogenetic sequence studied by VASSILIEVA & SMIRNOV (2001), a secondary mineralization of this
zone is improbable. Generally, in R. sibiricus
development of both characters (bicuspidity
and zone of division) seems more variable
and partly less conspicuous as in other Urodela.
4.2. The fate of dentigerous bones
during ontogeny and direction of dental
replacements
As in other Urodela, also in R. sibiricus development and replacement of the differently organized teeth takes place at different times
depending on the particular dentigerous bone
and its fate during further development.
Tooth replacement in all dentigerous bones,
typically is posterior to the tooth row in labial
direction. Development of dentigerous
bones of R. sibiricus and their degradation or
remodelling during metamorphosis was
thoroughly described by LEBEDKINA (summarized 1979, 2005, see also JÖMANN et al.
2005); the various tooth generations and their
temporally shifted development were illustrated by VASSILIEVA & SMIRNOV (2001). The
latter observations are deepened herein and
broadened with regard to the palatine and
the coronoid.
The typical sequence of differently shaped
tooth generations has been used to classify
“early” (see above), “late” larval teeth (mo-
212
nocuspid, “subpedicellate”) and “transformed” or “metamorphosed” teeth (see
above) in several Urodela including paedomorphic species (e.g., CLEMEN & GREVEN 1977,
1980, 1994; GREVEN & CLEMEN 1980). Initially, larval dentigerous bones of R. sibiricus bear
“non-pedicellate”, i.e., “early” larval teeth (see
also VASSILIEVA & SMIRNOV 2001). The later
the bone develops in ontogeny, the more
developed teeth (in the direction of the “late”
larval tooth) are established, i.e., very early
tooth stages are left out on bones developing
late in ontogenesis, e.g., on the maxilla. “Late”
larval teeth are first established on the premaxilla, then on the dentary and later on the
developing maxilla. At this time vomerine
and coronoid teeth (a single established
tooth in larva 3) were from the “early” larval
type. Palatinal teeth in larva 3 were, however,
lacking. It was shown by VASSILIEVA & SMIRNOV (2001) that the coronoid as well as the
palatinal dental laminae appear to be able to
produce short-lived “late” larval teeth
(named by the authors “subpedicellate”). Actually, we found “late” larval teeth on the coronoid of the specimens with delayed metamorphosis. The discrepancies regarding the
palatine may be attributed to our limited
material and the large variations suggested
for the development of dentition in R. sibiricus (see the discussion in V ASSILIEVA &
SMIRNOW 2001).
Metamorphosed bicuspid teeth are first
produced in the upper and lower jaw. All premaxillary and the most maxillary teeth of larva 4 in advanced metamorphosis had (incipient) bicuspids, whereas dentaries bore transformed teeth anteriorly and teeth of the “late”
larval type posteriorly, i.e., transformation of
teeth takes place from the anterior to posterior. The vomers still had “early” larval teeth.
After metamorphosis all systems still present
show bicuspid divided teeth. In larvae with
delayed metamorphosis all systems present
at this time had “late” larval teeth.
Regression of the palatinal tooth system
begins relatively early. This is stressed by the
fact that in the larvae with delayed metamorphosis palatinal teeth were totally absent (see
above). After multiple hibernation as assumed for R. sibiricus larvae (KUZMIN & THIESMEIER 2001; see the discussion in JÖMANN et
al., 2005), the palatine is separated from the
pterygoid, still fully developed, but free of
teeth. At this time the dental lamina of the
coronoid appeared still active.
Because of the relatively early degradation
of these dental laminae a subsequent delivery of new teeth ceases. This leads to a toothless palatine, either permanent when larvae
were hypopyhsectomized in time (Salamandra salamandra: CLEMEN 1978) or before complete resorption in course of metamorphosis when metamorphosis is delayed, e.g. by
deep temperatures (S. salamandra: CLEMEN
1978; R. sibiricus: JÖMANN et al. 2005; the present article). Degradation of the palatinal
portion of the palatopterygoid is considered
as one of the key factors indicating the onset
of metamorphosis (R EILLY 1986, 1987;
REILLY & ALTIG 1996). Onset, however, may
be indicated earlier, e.g., by the less conspicuous degradation of dental laminae.
In brief, regarding chronology of tooth replacements as well a disintegration of certain
dentigerous bones, R. sibiricus follows the
pattern realized in all urodeles hitherto examined that undergo metamorphosis. The typical spatial and temporal differences regarding development of fully transformed bicuspid teeth and their transitory stages (see
CLEMEN & GREVEN 1994 and the literature
cited above) in the various tooth systems is
very probably ascribed to different competences of the tooth producing tissue and its
different sensitivities to the metamorphosing
hormone (CLEMEN 1988 a, b; GREVEN & CLEMEN 1990).
Although briefly discussed in our previous
study (JÖMANN et al. 2005), we again discuss
herein the changes during remodelling of the
vomerine system around metamorphosis. In
most Urodela, these changes are remarkable
and have been long used for phylogenetic
considerations (e.g., LAURENT 1947; REGAL
1966; HECHT & EDWARDS 1977; ZHAO et al.
1988; CLEMEN & GREVEN 1994).
Apart from the fact that the larval vomer
of R. sibiricus bears several rows of teeth
rather than a single row (LEBEDKINA 1979,
2005; VASSILIEVA & SMIRNOV 2001; see above)
and that the vomerine tooth rows are less
parallel to the premaxillary arcade (see figures
in LEBEDKINA 2005 and JÖMANN et al. 2005),
the changes of the vomerine system during
transformation of R. sibiricus are less conspicuous as in many other Urodela (for review see
CLEMEN & GREVEN 1994). Metamorphosed
R. sibiricus have a nearly transverse vomerine
dentition more or less parallel to the upper
jaw arcade with a tooth replacement posterior to the tooth row in labial direction, i.e. the
labial replacement pattern is retained in transformed specimens. In other hynobiids more
conspicuous changes occur (e.g., ZHAO et al.,
1988; ADLER & ZHAO 1990; ZHANG et al. 2006).
Here the partes dentales form a short anterior,
transverse row and a longitudinal row directed posteriorly resulting in replacements posterior (in labial direction) to the transverse
tooth row and lateral (in lingual direction) to
the longitudinal tooth rows (GREVEN & CLEMEN 1985). The latter mode obviously has
evolved more than once in Urodela (see the
discussion in HECHT & EDWARDS 1977). R.
sibiricus shares the transversely orientation of
the vomerine dentition (and thus the posterior replacement of teeth) with the hynobiid genera Liua, Batrachuperus, Pachyhynobius,
Paradactylodon, and Onychodactylus (ZHAO et
al. 1988; ZHANG et al. 2006), which belong to
stream-type hynobiids and obviously do not
form a natural group (LARSON et al. 2003;
ZHANG et al. 2006). Transversely oriented vomerine teeth were said to hinder escape of
prey in those species feeding by suction in
water (ZHANG et al. 2006). These functional
suggestions do not contradict the assumption that a transverse tooth row with replacements in labial direction is a plesiomorphic
character of hynobiids and perhaps of all
213
Urodela (see the short discussion in JÖMANN
et al, 2005). Fossils from the Early Cretaceous
related to hynobiids, such as Liaoxitriton have
also a transverse arrangement of the vomerine teeth (WANG 2004).
4.3. Multiple rows versus a single row of
teeth
In the youngest larva available larvae (stage
16 according to LEBEDKINA’s table, l.c.; see
JÖMANN et al. 2005; late feeding larva according to VASSILIEVA & SMIRNOV 2001) we found
only on the palatine clear signs of two rows
of teeth without resorption pits. Dentaries,
premaxillae, and, when established, maxillae
bear a single row of teeth throughout ontogeny (VASSILIEVA & SMIRNOV 2001; LEBEDKINA
1979, 2005; JÖMANN et al. 2005) and postmetamorphosed specimens have a single row
of teeth on all dentigerous bones. LEBEDKINA (1979, 2005) draws a single row of teeth
on all dentigerous bones up to stage 7 with
the exception of the coronoid (early feeding
larva; see VASSILIEVA & SMIRNOV 2001). In her
stage 8 the palatine shows two rows of teeth
and two rows occur also on the vomer from
her stage 9 up to resorption in the premetamorphic period (stage 17). Our youngest
specimen did not clearly show two rows of
teeth on the vomers. These findings show
that already in “late feeding larvae” resorption of lateral margins of the vomer, but
also of the palatine and the coronoid has led
to the loss of teeth. In contrast to the findings of VASSILIEVA & SMIRNOW (2001) all teeth
of our specimen (stage 16) were from the
early larval type, i.e. monocuspid and entirely
undivided (see above). These discrepancies
may be attributed to individual variation.
According to our results and the findings
of VASSILIEVA & SMIRNOV (2001), the sequence
of tooth row numbers in the tooth systems
of R. sibiricus is as follows (the first functional dentition of a dentigerous bones necessarily comprises a single row): the upper
jaw and the dentary bear a single row through-
214
out ontogeny, the vomers bear up to three
rows in larvae and a single row in metamorphosed specimens. The coronoids bear up
to three rows, and the palatines up to two
rows that will be resorbed before metamorphosis. In other Urodela deviations from this
pattern occur mainly with respect to the premaxillae and palate (e.g. in Ambystomatidae,
where the palate is partly retained after metamorphosis) and vomer (e.g. in Plethodontidae) (see literature cited above).
Interestingly, the hynobiid, Onychodactylus
fischeri, which is now considered as sister
taxon of all other extant hynobiids (LARSON
et al. 2003; ZHANG et al. 2006) and which largely resembles R. sibiricus in the traits discussed herein, has a single row on all dentigerous
bones already in early developmental stages
(SMIRNOW & VASSILIEVA 2002).
at the onset of the lengthened late larval
period. The dental laminae of the coronoid
between vomer and palatine was, however,
still active at this time (see the picture in JÖMANN et al. 2005).
4.5. Conclusions
As shown herein and in previous articles of
various authors, the pattern of dentition, the
succession of differently shaped tooth generations, the direction of replacements and the
course and number of dental laminae (still
unknown in detail, but indirectly inferred from
gross morphology in part) of Ranodon. sibiricus, a representative of an ancient urodele
lineage, fits very well in the pattern present in
many other Urodela. The remodelling mainly
of the vomerine system during metamorphosis appears comparatively inconspicuous. We
suggest that many of the characters of the
4.4. Dental laminae
tooth systems summarized herein are highly
Knowledge of number and course of dental conserved plesiomorphic traits in Urodela.
laminae in larval and adult R. sibiricus is still
incomplete, but the available data and indi- Acknowledgements
rect evidence from the position and continuity of tooth rows allow for some conclusion. The technical help of Mrs. MARTINA FASEL
The upper jaw is accompanied by a conti- (Münster) and Mr. MARCEL BRENNER (Düsnuous dental lamina indicated by a conti- seldorf) is greatly appreciated.
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Accepted: 22.12. 2006

Greven J.mann Cleven.p65

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